Skip to main content
Log in

Duplication and divergence of the genes of the α-esterase cluster ofDrosophila melanogaster

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

The α-esterase cluster ofD. melanogaster contains 11 esterase genes dispersed over 60 kb. Embedded in the cluster are two unrelated open reading frames that have sequence similarity with genes encoding ubiquitin-conjugating enzyme and tropomyosin. The esterase amino acid sequences show 37–66% identity with one another and all but one have all the motifs characteristic of functional members of the carboxyl/cholinesterase multigene family. The exception has several frameshift mutations and appears to be a pseudogene. Patterns of amino acid differences among cluster members in relation to generic models of carboxyl/cholinesterase protein structure are broadly similar to those among other carboxyl/cholinesterases sequenced to date. However the α-esterases differ from most other members of the family in: their lack of a signal peptide; the lack of conservation in cysteines involved in disulfide bridges; and in four indels, two of which occur in or adjacent to regions that align with proposed substrate-binding sites of other carboxyl/cholinesterases. Phylogenetic analyses clearly identify three simple gene duplication events within the cluster. The most recent event involved the pseudogene which is located in an intron of another esterase gene. However, relative rate tests suggest that the pseudogene remained functional after the duplication event and has become inactive relatively recently. The distribution of indels also suggests a deeper node in the gene phylogeny that separates six genes at the two ends of the cluster from a block of five in the middle.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Beverley SM, Wilson AC (1984) Molecular evolution inDrosophila and the Higher Diptera. II A time scale for fly evolution. J Mol Evol 21:1–13

    Article  CAS  PubMed  Google Scholar 

  • Cavener DR, Ray SC (1991) Eukaryotic start and stop translation sites. Nucleic Acids Res 19:3185–3192

    CAS  PubMed  Google Scholar 

  • Collet C, Nielsen M, Russell RJ, Karl M, Oakeshott JG, Richmond RC (1990) Molecular analysis of duplicated esterase genes inDrosophila melanogaster. Mol Biol Evol 7:9–28

    CAS  PubMed  Google Scholar 

  • Cygler M, Schrag JD, Sussman JL, Harel M, Silman I, Gentry MK, Doctor BP (1993) Relationship between sequence conservation and three dimensional structure in a large family of esterases, lipases, and related proteins. Protein Sci 2:366–382

    CAS  PubMed  Google Scholar 

  • Felsenstein J (1991) Phylip. University of Washington, Seattle

    Google Scholar 

  • Field LM, Williamson MS, Moores GD, Devonshire AL (1993) Cloning and analysis of the esterase genes conferring insecticide resistance in the peach-potato aphidMyzus persicae (Sulzer). Biochem J 294:569–574

    CAS  PubMed  Google Scholar 

  • Genetics Computer Group (1994) GCG version 8.0.575 Science Drive, Madison, WI 53711, USA

  • Gillespie JH, Kojima K (1968) The degree of polymorphism in enzymes involved in energy production compared to that in nonspecific enzymes in twoDrosophila ananassae populations. Genetics 61:582–585

    CAS  Google Scholar 

  • Graham GJ (1995) Tandem genes and clustered genes. J Theor Biol 175:71–87

    Article  CAS  PubMed  Google Scholar 

  • Harel M, Sussman JL, Krejci E, Bon S, Chanal P, Massoulie J, Silman I (1992) Conversion of acetylcholinesterase to butyrylcholinesterase: modeling and mutagenesis. Proc Natl Acad Sci USA 89: 10827–10831

    CAS  PubMed  Google Scholar 

  • Healy MJ, Dumancic MM, Oakeshott JG (1991) Biochemical and physiological studies of soluble esterases fromDrosophila melanogaster. Biochem Genet 29:365–388

    Article  CAS  PubMed  Google Scholar 

  • Hughes PB, Raftos DA (1985) Genetics of an esterase associated with resistance to organophosphorus insecticides in the sheep blowfly,Lucilia cuprina (Wiedemann) (Diptera:Calliphoridae). Bull Entomol Res 75:535–544

    CAS  Google Scholar 

  • Jentsch S, Seufert W, Sommer T, Reins H-A (1990) Ubiquitin-conjugating enzymes: novel regulators of eukaryotic cells. Trends Biochem Sci 15:195–198

    Article  CAS  PubMed  Google Scholar 

  • Jones G, Venkataraman V, Ridley B, O'Mahony P, Turner H (1994) Structure, expression and gene sequence of a juvenile hormone esterase-related protein from metamorphosing larvae ofTrichoplusia ni. Biochem J 302:827–835

    CAS  PubMed  Google Scholar 

  • Kumar S, Tamura K, Nei M (1993) MEGA: Molecular Evolutionary Genetics Analysis version 1.0. The Pennsylvania State University, University Park, PA 16802

    Google Scholar 

  • Lotti M, Grandori R, Fusetti F, Longhi S, Brocca S, Tramontano A, Alberghina L (1993) Cloning and analysis ofCandida cylindracea lipase sequences. Gene 124:45–55

    Article  CAS  PubMed  Google Scholar 

  • Morton RA, Singh RS (1985) Biochemical properties, homology, and genetic variation ofDrosophila “non-specific” esterases. Biochem Genet 23:959–972

    Article  CAS  PubMed  Google Scholar 

  • Mouchès C, Pauplin Y, Agarwal M, Lemieux L, Herzog M, Abadon M, Beyssat-Arnaouty V, Hyrien O, de Saint Vincent BR, Georghiou GP, Pasteur N (1990) Characterization of amplification core and esterase B1 gene responsible for insecticide resistance inCulex. Proc Natl Acad Sci USA 87:2574–2578

    PubMed  Google Scholar 

  • Mount SM, Burks C, Hertz G, Stormo GD, White O, Fields C (1992) Splicing signals inDrosophila: intron size, information content, and consensus sequences. Nucleic Acids Res 20:4255–4262

    CAS  PubMed  Google Scholar 

  • Mutero A, Pralavorio M, Bride J-M, Fournier D (1994) Resistance associated point mutations in insecticide-insensitive acetylcholinesterase. Proc Natl Acad Sci USA 91:5922–5926

    CAS  PubMed  Google Scholar 

  • Oakeshott JG, van Papenrecht EA, Boyce TM, Healy MJ, Russell RJ (1993) Evolutionary genetics ofDrosophila esterases. Genetica 90: 239–268

    Article  CAS  PubMed  Google Scholar 

  • Ollis DL, Cheah E, Cygler M, Dijkstra B, Frolow F, Franken SM, Harel M, Remington SJ, Silman I, Schrag J, Sussman JL, Verschueren KHG, Goldman A (1992) The α/β hydrolase fold. Protein Eng 5:197–211

    CAS  PubMed  Google Scholar 

  • Powell JR, DeSalle R (1995)Drosophila molecular phylogenies and their uses. In: Hecht MK (ed) Evolutionary biology. Plenum Press, p 88–137

  • Prestridge DS (1991) Signal scan; a computer program that scans DNA sequences for eukaryotic transcriptional elements. Comput Appl Biosci 7:203–206

    CAS  PubMed  Google Scholar 

  • Riley M (1989) Nucleotide sequence of theXdh region in Drosophila pseudoobscura and an analysis of the evolution of synonymous codons. Mol Biol Evol 6:33–52

    CAS  PubMed  Google Scholar 

  • Ripoll DR, Faerman CH, Axelsen PH, Silman I, Sussman JL (1993) An electrostatic mechanism for substrate guidance down the aromatic gorge of acetylcholinesterase. Proc Natl Acad Sci USA 90:5128–5132

    CAS  PubMed  Google Scholar 

  • Rost B, Sander C (1993) Prediction of protein structure at better than 70% accuracy. J Mol Biol 232:584–599

    Article  CAS  PubMed  Google Scholar 

  • Russell RJ, Robin GC, Kostakos P, Newcomb RD, Boyce TM, Medveczky KM, Oakeshott JG (1996) Molecular cloning of an a esterase gene cluster on chromosome 3R ofDrosophila melanogaster. Insect Biochem Mol Biol 26:235–247

    CAS  PubMed  Google Scholar 

  • Sayle R (1994) RasMac molecular graphics. Modular CHEM Consortium

  • Schumacher M, Camp S, Maulet Y, Newton M, MacPhee-Quigley K, Taylor SS, Friedman T, Taylor P (1986) Primary structure ofTorpedo californica acetylcholinesterase deduced from its cDNA sequence. Nature 319:407–409

    Article  CAS  PubMed  Google Scholar 

  • Shrag JD, Cygler M (1993) 1.8A refined structure of the lipase fromGeotrichum candidum. J Mol Biol 230:575–591

    Google Scholar 

  • Smyth KA, Russell RJ, Oakeshott JG (1994) A cluster of at least three esterase genes inLucilia cuprina includes malathion carboxylesterase and two other esterase genes implicated in resistance to organophosphates. Biochem Genet 32:437–453

    Article  CAS  PubMed  Google Scholar 

  • Spackman ME, Oakeshott JG, Smyth K-A, Medveczky KM, Russell RJ (1994) A cluster of esterase genes on chromosome 3R ofDrosophila melanogaster includes homologues of esterase genes conferring insecticide resistance inLucilia cuprina. Biochem Genet 32:39–62

    Article  CAS  PubMed  Google Scholar 

  • Sullivan DT, Starmer WT, Curtiss SW, Menotti-Raymond M, Yum J (1994) Unusual molecular evolution of anAdh pseudogene inDrosophila. Mol Biol Evol 11:443–458

    CAS  PubMed  Google Scholar 

  • Sussman JL, Harel M, Frolow F, Oefner C, Goldman A, Toker L, Silman I (1991) Atomic structure of acetylcholinesterase fromTorpedo califomica: a prototypic acetylcholine-binding protein. Science 253:872–879

    CAS  PubMed  Google Scholar 

  • Swofford DL (1993) PAP: Phylogenetic analysis using parsimony. Illinois Natural History Survey, Champaign, IL

    Google Scholar 

  • Swofford DL, Begle DP (1993) Paup manual. Lab. of Molecular systematics, Smithsonian Institute

  • Tajima F (1993) Simple methods for testing the molecular evolutionary clock hypothesis. Genetics 135:599–607

    CAS  PubMed  Google Scholar 

  • Vaughan A, Hemingway J (1995) Mosquito carboxylesterase Estα2 (A2). J Biol Chem 270:17044–17049

    Article  CAS  PubMed  Google Scholar 

  • Vellom DC, Radic Z, Li Y, Pickering NA, Camp S, Taylor P (1993) Amino acid residues controlling acetylcholinesterase and butyryl-cholinesterase specificity. Biochemistry 32:12–17

    Article  CAS  PubMed  Google Scholar 

  • Villani F, White GB, Curtis CF, Miles SJ (1983) Inheritance and activity of some esterases associated with organophosphate resistance in mosquitoes of the complex ofCulex pipiens L. (Diptera: Culicidae). Bull Entomol Res 23:154–170

    Google Scholar 

  • von Heijne G (1986) A new method for predicting signal sequence cleavage sites. Nucleic Acids Res 14:4683–4691

    Google Scholar 

  • Weller GL, Foster GG (1993) Genetic maps of the sheep blowflyLucilia cuprina: linkage group correlations with other dipteran genera. Genome 36:495–506

    CAS  PubMed  Google Scholar 

  • Wirth MC, Marquine M, Georghiou GP, Pasteur N (1990) Esterases A2 and B2 inCulex quinquefasciatus (Diptera: Culicidae). Role in organophosphate resistance and linkage studies. J Med Entomol 7:202–206

    Google Scholar 

  • Wright TRF, Maelmyre R (1963) A homologous gene/enzyme system. Esterase 6 inDrosophila melanogaster andDrosophila simulans. Genetics 48:1717–1726

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Correspondence to: C. Robin

Rights and permissions

Reprints and permissions

About this article

Cite this article

Robin, C., Russell, R.J., Medveczky, K.M. et al. Duplication and divergence of the genes of the α-esterase cluster ofDrosophila melanogaster . J Mol Evol 43, 241–252 (1996). https://doi.org/10.1007/BF02338832

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02338832

Key words

Navigation